Is a mollusc an evolved bent metatrochophore? A histochemical investigation of neurogenesis in Mytilus (Mollusca: Bivalvia)

Abstract

Acetylcholinesterase (AChE) activity, a marker of neural differentiation, was histo-chemically localized in embryos and larvae of Mytilus galloprovincialis Lamarck and M. edulis L. (Mollusca: Bivalvia). The results show that: (1) the first AChE-active cells develop as two bilaterally symmetrical, postero-dorsal pioneer sensory neurons and their supporting superficial cells; (2) the pathways of their pioneering longitudinal axons are the same as those of two bilaterally symmetrical nerve cords which differentiate later in a postero-anterior direction; (3) in the conchostoma larva the posterior neurons and their associated superficial AChE-active cells give rise to two ciliary sensory-like organs which are the earliest rudiments of pedal ganglia and primary byssus glands; (4) three pairs of posttrochal gangliar rudiments, most probably visceral, parietal and pleural ganglia, develop on the same longitudinal nerve cords in the trochophore larva; (5) starting from the veliger stage, the presumptive foot rotates on the ventral side and migrates forwards, so that this gangliar chain is bent and the viscero-parietal ganglia become localized dorso-posteriorly to the pedal ganglia; (6) the cerebral ganglia differentiate together with the apical organ and the nerve network of the velum after the first pedal nerve rudiments have been detected.

Histochemical localization of FMRFamide, serotonin and catecholamines in embryonic Crepidula fornicata (Gastropoda, Prosobranchia)

“…Velar innervation had been thought to originate from the cerebral ganglia (Arkett et al 1987;Carter 1926Carter , 1928Mackie et al 1976), but more recently it has been shown that axons may actually emerge from cells of the apical organ in some of the Opisthobranchia (Kempf et al 1997;Marois and Carew 1997a-c) and I. obsoleta (Prosobranchia; see Lin and Leise 1996a, b). In addition, velar innervation has also been reported from cells that may comprise an apical organ in M. edulis (Bivalvia; see Croll et al 1997;Kulakovskiy and Flyachinskaya 1994;Raineri 1995;Raineri and Ospovat 1994). Although the origin of velar innervation could not be determined in C. fornicata from this present study, it is likely that such extensive innervation arises from the apical cells since fibers were observed in velar regions prior to the first cells of the cerebral or pedal ganglia.…”

“…An apical organ has been reported in some of the Gastropoda (Bonar 1977(Bonar , 1978Chia and Koss 1984;Kempf et al 1991Kempf et al , 1997Lin and Leise 1996a, b;Marois and Carew 1997c;Moor 1983;Page 1993;Raineri 1995;Raineri and Ospovat 1994) and the Bivalvia (Raineri 1995;Raineri and Ospovat 1994) as well as many other swimming invertebrate larvae (see for example, Hay- Schmidt 1990a-c, 1995Lacalli 1981Lacalli , 1994. In many molluscs (Bonar 1978;Chia and Koss 1984;Kempf et al 1997;Leise 1996;Marois and Carew 1997a, b) and other invertebrates (see Lacalli 1994), the apical organ possesses flask-or vase-shaped cells with protruding cilia at the epithelial surface.…”

“…The FMRFamide-LIR and serotonin-LIR cells in these various species appeared in early stages prior to the first cells of the cerebral ganglia. Neuronal elements located outside the region of the future adult central nervous system (CNS) have also been identified in early larval stages from the Bivalvia using techniques to localize acetylcholinesterase, catecholamines, and serotonin (Croll et al 1997;Kulakovskiy and Flyachinskaya 1994;Raineri 1995;Raineri and Ospovat 1994). The presence of such early elements suggests the possibility that the Mollusca possess larval nervous systems which appear early in development and can become relatively extensive, but that have gone largely unrecognized in the past.…”

Neuronal development in larval mussel Mytilus trossulus (Mollusca: Bivalvia)

“…The few studies that have focused on bivalves to date have examined only restricted developmental stages and/or employed histochemical staining techniques with limited resolution and questionable speciWcity (Ospovat et al 1989;Koolakovsky and Phlyachinskaya 1993;Raineri and Ospovat 1994;Raineri 1995). Although 5-HT-containing neuronal elements have been observed in the apical region of the bivalves Mytilus edulis (Linné 1758) (Croll et al 1997;Flyachinskaya 2000) and Spisula solidissima (Dillwyn 1817) (Kreiling et al 2001), the exact locations of these cells in the larval apical organ versus the cerebral ganglia are unclear.…”

“…On one hand, bivalves are generally considered more closely related phylogenetically to gastropods than to polyplacophorans (see Taylor 1996), while on the other hand, the nervous system of the trochophore of M. edulis has been suggested to closely resemble that of a larval annelid (Raineri 1995;Nielsen 2001). The anatomy of the adult annelid nervous system, however, more closely resembles (at least superWcially) that of polyplacophorans, rather than bivalves (Bullock and Horridge 1965;Beklemishev 1969).…”